Abstract
We describe a new member of the class of mutants in Arabidopsis exhibiting high rates of cyclic electron flow around photosystem I (CEF), a light-driven process that produces ATP but not NADPH. High cyclic electron flow 2 (hcef2) shows strongly increased CEF activity through the NADPH dehydrogenase complex (NDH), accompanied by increases in thylakoid proton motive force (pmf), activation of the photoprotective qE response, and the accumulation of H2O2. Surprisingly, hcef2 was mapped to a non-sense mutation in the TADA1 (tRNA adenosine deaminase arginine) locus, coding for a plastid targeted tRNA editing enzyme required for efficient codon recognition. Comparison of protein content from representative thylakoid complexes, the cytochrome bf complex, and the ATP synthase, suggests that inefficient translation of hcef2 leads to compromised complex assembly or stability leading to alterations in stoichiometries of major thylakoid complexes as well as their constituent subunits. Altered subunit stoichiometries for photosystem I, ratios and properties of cytochrome bf hemes, and the decay kinetics of the flash-induced thylakoid electric field suggest that these defect lead to accumulation of H2O2 in hcef2, which we have previously shown leads to activation of NDH-related CEF. We observed similar increases in CEF, as well as increases in H2O2 accumulation, in other translation defective mutants. This suggests that loss of coordination in plastid protein levels lead to imbalances in photosynthetic energy balance that leads to an increase in CEF. These results taken together with a large body of previous observations, support a general model in which processes that lead to imbalances in chloroplast energetics result in the production of H2O2, which in turn activates CEF. This activation could be from either H2O2 acting as a redox signal, or by a secondary effect from H2O2 inducing a deficit in ATP.
Highlights
IntroductionLight is harvested by two distinct photochemical reaction centers, photosystem II (PSII) and photosystem I (PSI) that stimulate electron transfer through series of redox carriers to store solar energy in forms to drive biochemical processes (Eberhard et al, 2008)
This work arose out of our attempts to understand how chloroplasts balance their energy budgets to efficiently capture solar energy and provide plants with sufficient energy for growth and maintenance while avoiding self-destructive side reactions, which led us to find unexpected connections between the maintenance of photosynthesis, the regulation of rigid stoichiometries of protein complexes in the chloroplast and the production of the reactive oxygen species H2O2.In oxygenic photosynthesis, light is harvested by two distinct photochemical reaction centers, photosystem II (PSII) and photosystem I (PSI) that stimulate electron transfer through series of redox carriers to store solar energy in forms to drive biochemical processes (Eberhard et al, 2008)
When PSI and PSII are electronically connected in series, they drive linear electron flow (LEF), which results in the oxidation of water and the reduction of NADPH
Summary
Light is harvested by two distinct photochemical reaction centers, photosystem II (PSII) and photosystem I (PSI) that stimulate electron transfer through series of redox carriers to store solar energy in forms to drive biochemical processes (Eberhard et al, 2008). When PSI and PSII are electronically connected in series, they drive linear electron flow (LEF), which results in the oxidation of water and the reduction of NADPH. The electron transfer reactions of LEF are coupled to the uptake of protons from the chloroplast stroma and their deposition into the lumen, establishing an electrochemical gradient of protons, or proton motive force (pmf ). Protons are released into the lumen during water oxidation at the oxygen-evolving complex (OEC) of PSII and during plastoquinol oxidation at the Qo site of the cytochrome bf complex. The pmf generated in these electron and proton transfer reactions drives the synthesis of ATP at the chloroplast ATP synthase
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